Autonomic impairment in Alzheimer’s disease is revealed by complexity analysis of functional thermal imaging signals during cognitive tasks

OBJECTIVE Alzheimer's disease (AD) is characterized by progressive memory failures and visuospatial impairment. Moreover, AD can be accompanied by autonomic system alterations, which, among other impacts, affect thermoregulatory activity. We here investigate differences in autonomic activity between AD patients and healthy controls (HC), employing a complexity analysis of functional infrared imaging (fIRI) data acquired at rest and during the execution of clinical cognitive and mnemonic tests. APPROACH fIRI allows for contactless monitoring of autonomic activity and its thermoregulatory expression without interfering with the psychophysiological state of the subject, preserving free interaction with the doctor. The signal complexity analysis, based on the sample entropy, was compared to a standard frequency-based analysis of autonomic-related signals. MAIN RESULTS AD patients exhibited lower complexity of fIRI signals during the tests, which could be indicative of a stronger sympathetic activity with respect to HC. No significant effects were found at rest. No differences were found on employing frequency-based analysis. SIGNIFICANCE This study confirms that AD patients may exhibit peculiar autonomic responses associated with the execution of cognitive tasks that can be measured through fIRI. Moreover, these responses could be highlighted by a nonlinear metric of signal predictability such as the sample entropy establishing autonomic impairment of AD patients.

[1]  Moses O. Sokunbi,et al.  Nonlinear Complexity Analysis of Brain fMRI Signals in Schizophrenia , 2014, PloS one.

[2]  Gennaro Pagano,et al.  Autonomic dysfunction in Alzheimer's disease: tools for assessment and review of the literature. , 2014, Journal of Alzheimer's disease : JAD.

[3]  M Revach,et al.  Increased sympathetic and decreased parasympathetic cardiac innervation in patients with Alzheimer's disease. , 1992, Archives of neurology.

[4]  D. Linden,et al.  Resting state fMRI entropy probes complexity of brain activity in adults with ADHD , 2013, Psychiatry Research: Neuroimaging.

[5]  A. Merla,et al.  Biomedical Applications of Functional Infrared Imaging , 2005, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

[6]  P. Scheltens,et al.  Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS–ADRDA criteria , 2007, The Lancet Neurology.

[7]  Michael Anbar,et al.  Assessment of Physiologic and Pathologic Radiative Heat Dissipation Using Dynamic Infrared Imaging , 2002, Annals of the New York Academy of Sciences.

[8]  J. Molinuevo,et al.  International Work Group criteria for the diagnosis of Alzheimer disease. , 2013, The Medical clinics of North America.

[9]  J. Rosenbek,et al.  Swallowing Dysfunction and Autonomic Nervous System Dysfunction in Alzheimer's Disease: A Scoping Review of the Evidence , 2013, Journal of the American Geriatrics Society.

[10]  Joseph D. Bronzino,et al.  Medical Infrared Imaging : Principles and Practices , 2012 .

[11]  M. Eysenck,et al.  Anxiety and cognitive performance: attentional control theory. , 2007, Emotion.

[12]  E. Ring,et al.  Infrared thermal imaging in medicine , 2012, Physiological measurement.

[13]  Roberto Hornero,et al.  Analysis of electroencephalograms in Alzheimer's disease patients with multiscale entropy. , 2006 .

[14]  Arcangelo Merla,et al.  Assessment of the Autonomic Response in Alzheimer's Patients During the Execution of Memory Tasks: A Functional Thermal Imaging Study. , 2018, Current Alzheimer research.

[15]  D. Abásolo,et al.  Entropy analysis of the EEG background activity in Alzheimer's disease patients , 2006, Physiological measurement.

[16]  D. Benson,et al.  Dementia of the Alzheimer Type , 1986, Journal of the American Geriatrics Society.

[17]  E. Salazar-López,et al.  The mental and subjective skin: Emotion, empathy, feelings and thermography , 2015, Consciousness and Cognition.

[18]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

[19]  J. Sato,et al.  Thermoregulatory profile of neurodegeneration‐induced dementia of the Alzheimer's type using intracerebroventricular streptozotocin in rats , 2018, Acta physiologica.

[20]  P. Mcgeer,et al.  Increase in Core Body Temperature of Alzheimer’s Disease Patients as a Possible Indicator of Chronic Neuroinflammation: A Meta-Analysis , 2006, Gerontology.

[21]  A D Baddeley,et al.  The decline of working memory in Alzheimer's disease. A longitudinal study. , 1991, Brain : a journal of neurology.

[22]  M. Vitiello,et al.  Entrained Body Temperature Rhythms Are Similar in Mild Alzheimer's Disease, Geriatric Onset Depression, and Normal Aging , 1992, Journal of geriatric psychiatry and neurology.

[23]  J. Escudero,et al.  Analysis of MEG Background Activity in Alzheimer’s Disease Using Nonlinear Methods and ANFIS , 2009, Annals of Biomedical Engineering.

[24]  A L Goldberger,et al.  Physiological time-series analysis: what does regularity quantify? , 1994, The American journal of physiology.

[25]  A. Malliani,et al.  Power spectrum analysis of heart rate variability: a tool to explore neural regulatory mechanisms. , 1994, British heart journal.

[26]  Yoshihisa Fujiwara,et al.  Using facial skin temperature to objectively evaluate sensations , 1997 .

[27]  D. Carrettiero,et al.  Current understanding on the neurophysiology of behavioral thermoregulation , 2015, Temperature.

[28]  A. Rey L'examen psychologique dans les cas d'encéphalopathie traumatique. (Les problems.). , 1941 .

[29]  A. Merla,et al.  Mom feels what her child feels: thermal signatures of vicarious autonomic response while watching children in a stressful situation , 2013, Front. Hum. Neurosci..

[30]  P. Remy,et al.  Executive function deficits in early Alzheimer's disease and their relations with episodic memory. , 2006, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[31]  P. Diamond,et al.  Thermoregulatory Behavior in Alzheimer's Disease , 1991, Journal of the American Geriatrics Society.

[32]  Marc Garbey,et al.  Contact-Free Measurement of Cardiac Pulse Based on the Analysis of Thermal Imagery , 2007, IEEE Transactions on Biomedical Engineering.

[33]  Jody Clay-Warner,et al.  Infrared Thermography as a Measure of Emotion Response , 2015 .

[34]  João Carlos Bouzas Marins,et al.  Classification of factors influencing the use of infrared thermography in humans: A review , 2015 .

[35]  A. Marette,et al.  Impaired thermoregulation and beneficial effects of thermoneutrality in the 3×Tg-AD model of Alzheimer's disease , 2016, Neurobiology of Aging.

[36]  Alan V. Sahakian,et al.  Use of Sample Entropy Approach to Study Heart Rate Variability in Obstructive Sleep Apnea Syndrome , 2007, IEEE Transactions on Biomedical Engineering.

[37]  E. Stopa,et al.  Circadian locomotor activity and core-body temperature rhythms in Alzheimer's disease , 1995, Neurobiology of Aging.

[38]  R. Vardasca,et al.  Current Issues in Medical Thermography , 2013 .

[39]  A. Reinberg,et al.  Age-related changes in both circadian and seasonal rhythms of rectal temperature with special reference to senile dementia of Alzheimer type. , 1986, Gerontology.

[40]  D. Carrettiero,et al.  Temperature and toxic Tau in Alzheimer's disease: new insights , 2015, Temperature.

[41]  M. Sillero-Quintana,et al.  Circadian and gender differences in skin temperature in militaries by thermography , 2015 .

[42]  Michele Zito,et al.  Complexity of Frontal Cortex fNIRS Can Support Alzheimer Disease Diagnosis in Memory and Visuo-Spatial Tests , 2019, Entropy.

[43]  M. P. Griffin,et al.  Sample entropy analysis of neonatal heart rate variability. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[44]  Michele Zito,et al.  Study of memory deficit in Alzheimer’s disease by means of complexity analysis of fNIRS signal , 2017, Neurophotonics.

[45]  K. Newell,et al.  Changing complexity in human behavior and physiology through aging and disease , 2002, Neurobiology of Aging.

[46]  D. Cuesta-Frau,et al.  Characterization of Sample Entropy in the Context of Biomedical Signal Analysis , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[47]  J. Halter,et al.  Impaired sympathetic nervous system response to cognitive effort in early Alzheimer's disease. , 1989, Journal of gerontology.

[48]  B. Winblad,et al.  Autonomic dysfunction in Alzheimer's disease , 1995, Acta neurologica Scandinavica.

[49]  George T. Grossberg,et al.  Circadian Rhythm Disturbances in Patients with Alzheimer's Disease: A Review , 2010, International journal of Alzheimer's disease.

[50]  S. Cappa,et al.  Visual and spatial perception in the early phase of Alzheimer's disease. , 1998, Neuropsychology.

[51]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[52]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[53]  Wuon-Shik Kim,et al.  Nonlinear characteristics of heart rate time series: influence of three recumbent positions in patients with mild or severe coronary artery disease , 2005, Physiological measurement.

[54]  Arcangelo Merla,et al.  New Frontiers for Applications of Thermal Infrared Imaging Devices: Computational Psychopshysiology in the Neurosciences , 2017, Sensors.